Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis
Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins,...
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| Vydáno v: | Cell Ročník 185; číslo 12; s. 2148 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
09.06.2022
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| ISSN: | 1097-4172, 1097-4172 |
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| Abstract | Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking. |
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| AbstractList | Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking. Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking. |
| Author | Munneke, Matthew J Monteith, Andrew J Edmonds, Katherine A Beavers, William N Skaar, Eric P DiMarchi, Richard D Thalluri, Kishore Caprioli, Richard M Rodríguez Nassif, Aslin M Wu, Hongwei Krystofiak, Evan S Perera, Yasiru R Murdoch, Caitlin C Petoletti, Amber M Drury, Sydney L Kruse, Angela R S Chazin, Walter J Weiss, Andy Jordan, Matthew R Spraggins, Jeffrey M Giedroc, David P |
| Author_xml | – sequence: 1 givenname: Andy surname: Weiss fullname: Weiss, Andy organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 2 givenname: Caitlin C surname: Murdoch fullname: Murdoch, Caitlin C organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 3 givenname: Katherine A surname: Edmonds fullname: Edmonds, Katherine A organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 4 givenname: Matthew R surname: Jordan fullname: Jordan, Matthew R organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 5 givenname: Andrew J surname: Monteith fullname: Monteith, Andrew J organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 6 givenname: Yasiru R surname: Perera fullname: Perera, Yasiru R organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA – sequence: 7 givenname: Aslin M surname: Rodríguez Nassif fullname: Rodríguez Nassif, Aslin M organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA – sequence: 8 givenname: Amber M surname: Petoletti fullname: Petoletti, Amber M organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 9 givenname: William N surname: Beavers fullname: Beavers, William N organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 10 givenname: Matthew J surname: Munneke fullname: Munneke, Matthew J organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 11 givenname: Sydney L surname: Drury fullname: Drury, Sydney L organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA – sequence: 12 givenname: Evan S surname: Krystofiak fullname: Krystofiak, Evan S organization: Cell Imaging Shared Resource, Vanderbilt University, Nashville, TN 37232, USA – sequence: 13 givenname: Kishore surname: Thalluri fullname: Thalluri, Kishore organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 14 givenname: Hongwei surname: Wu fullname: Wu, Hongwei organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 15 givenname: Angela R S surname: Kruse fullname: Kruse, Angela R S organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA – sequence: 16 givenname: Richard D surname: DiMarchi fullname: DiMarchi, Richard D organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 17 givenname: Richard M surname: Caprioli fullname: Caprioli, Richard M organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA – sequence: 18 givenname: Jeffrey M surname: Spraggins fullname: Spraggins, Jeffrey M organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA; Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37232, USA – sequence: 19 givenname: Walter J surname: Chazin fullname: Chazin, Walter J organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA – sequence: 20 givenname: David P surname: Giedroc fullname: Giedroc, David P email: giedroc@indiana.edu organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA. Electronic address: giedroc@indiana.edu – sequence: 21 givenname: Eric P surname: Skaar fullname: Skaar, Eric P email: eric.skaar@vumc.org organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA. Electronic address: eric.skaar@vumc.org |
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| Keywords | metalloprotein zf-C6H2 CBWD ZNG1 metallochaperone zinc finger GTPase zinc COG0523 METAP1 |
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| References | 35918525 - Nature. 2022 Aug;608(7921):38-39. doi: 10.1038/d41586-022-01988-2 35688131 - Cell. 2022 Jun 9;185(12):2013-2015. doi: 10.1016/j.cell.2022.05.012 |
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| SubjectTerms | Animals GTP Phosphohydrolases - metabolism Homeostasis Metallochaperones - metabolism Metalloendopeptidases - metabolism Metalloproteins - genetics Mice Zebrafish - metabolism Zinc - metabolism |
| Title | Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis |
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